The role of size-specific predation in the evolution and diversification of prey life histories

Some of the best empirical examples of life-history evolution involve responses to predation. Nevertheless, most life-history theory dealing with responses to predation has not been formulated within an explicit dynamic food-web context. In particular, most previous theory does not explicitly consider the coupled population dynamics of the focal species and its predators and resources. Here we present a model of life-history evolution that explores the evolutionary consequences of size-specific predation on small individuals when there is a trade-off between growth and reproduction. The model explicitly describes the population dynamics of a predator, the prey of interest, and its resource. The selective forces that cause life-history evolution in the prey species emerge from the ecological interactions embodied by this model and can involve important elements of frequency dependence. Our results demonstrate that the strength of the coupling between predator and prey in the community determines many aspects of life-history evolution. If the coupling is weak (as is implicitly assumed in many previous models), differences in resource productivity have no effect on the nature of life-history evolution. A single life-history strategy is favored that minimizes the equilibrium resource density (if possible). If the coupling is strong, then higher resource productivities select for faster growth into the predation size refuge. Moreover, under strong coupling it is also possible for natural selection to favor an evolutionary diversification of life histories, possibly resulting in two coexisting species with divergent life-history strategies.     

The evolution of rates of successful and unsuccessful predation

Summary The question, how will evolutionary change in a predator or in its prey change the ratio of the rate of successful captures to the rate of unsuccessful capture attempts is addressed. I argue that this ratio is not a good index of the predator's adaptation to prey capture, because decreased costs of capture attempts or increased assimilation efficiency (both favored by natural selection in the predator) will usually reduce the ratio. In addition, the evolution of increased ability to capture prey may lead to a reduction in the success/failure ratio. Analysis of several simple models suggests that this result is robust. The presence of unsuccessful predation does have an important influence on the evolution of predator traits that increase its rate of encounter with the prey; the presence of unsuccessful predation may cause the predator to increase its adaptations for prey detection in response to an increase in the prey's ability to avoid detection.     

Stream drift as a consequence of disturbance by invertebrate predators

Summary We carried out an experimental field study in a Swedish stream in order to determine whether mobile predators enhance the drift of stream insects. We increased the density of nymphs of the predaceous perlid stonefly, Dinocras cephalotes, in an experimental section of a stream up to densities in another more densely populated part of the same stream. The drift of several benthic species increased significantly compared to a control section where D. cephalotes were rare. Experiments carried out in September showed a strongly elevated drift response in nymphs of the mayfly Baetis rhodani only, whereas May experiments resulted in increased drift in B. rhodani as well as the amphipod Gammarus pulex, the stonefly Leuctra fusca, chironomids, and the total number of drifting animals. In September, we found that the drift response of Baetis rhodani to predator disturbance was dependent on the size of mayfly nymphs; small nymphs appeared in greater numbers in the drift nets than did large nymphs. A subsequent laboratory analysis of drift lengths of B. rhodani nymphs supported the hypothesis that small nymphs travel in the drift for longer than do large nymphs, particularly in darkness. We suggest that morphological constraints in vision or swimming performance, or both, cause small nymphs to drift longer. In May, size-dependent drift was less obvious, probably because the size of the nymphs was considerably greater than in September.     

Egg-brooding, body size and predation risk in planktonic marine copepods

We investigated the interacting effects of copepod body size and the presence or absence of egg masses on the risk of predation by a visual predator. We conducted selection experiments involving three-spined sticklebacks (Gasterosteus aculeatus) and copepods ranging in body mass from 0.5 to 740 μg C: Oithona similis, Corycaeus anglicus, Pseudocalanus newmani, P. moultoni, Pseudodiaptomus marinus, and Paraeuchaeta elongata. We found that sticklebacks selected ovigerous females of the two smallest-bodied species of copepods (Oithona similis and Corycaeus anglicus). In contrast, the fish showed no significant selection for ovigerous females of the remaining, larger-bodied species. Unexpectedly, egg mass position (i.e., in a ventral, dorsal or lateral location on the urosome) appeared to influence predation risk more than did body size, resulting in higher predation risk for the cyclopoid and poecilostomatoid species than for the calanoid species we tested. Although the sticklebacks showed no statistically significant preference for ovigerous females of any of the four calanoid species, for each species the overall proportion of ovigerous females ingested was slightly greater than 0.50. Thus, whether body size influences the susceptibility of egg-brooding calanoid copepods to predation remains an open question. Received: 24 August 1998 / Accepted: 6 July 1999     

Fluid-mediated dispersal in streams: models of settlement from the drift

I propose proximal mechanisms that help explain, unify, and expand the predictions of widely accepted empirical models of settlement in streams. I separated the process that leads to settlement of a drifting particle into three stages: (1) initial contact with a substrate, (2) attachment, and (3) settlement sensu stricto. I used physical principles (height above the bed, sinking rate, current speed profile) to predict time until contact (stage 1). I compared these predictions with empirical measurements of settlement of individual black fly larvae (Simulium vittatum) in a laboratory flume. I developed models from empirical data for stages 2 and 3. Each of these models is individual-based and predicts the fate of a single individual. To obtain a population level prediction, models for the three stages were combined and used to simulate the settlement of a group of black fly larvae. The predictions of this simulation were qualitatively similar to population level data from the literature particularly after the incorporation of channel-wide spatial heterogeneity in current speed. The effect of flow heterogeneity on the model agrees with previous work on the lateral transport of stream invertebrates during drift events showing that many organisms settle preferentially in slower areas. By using proximal principles, the approach used in this study brings into focus basic parameters and processes that influence settlement at the scale of the organisms. It also provides a null hypothesis against which to study the effect of local flow heterogeneity on the settlement of stream invertebrates and the capacity of organisms to actively influence settlement. Water currents in streams and rivers commonly transport large numbers of organisms. Consequently, hydrodynamic factors that favor or hamper the settlement of these organisms can potentially influence distributions and abundance. Moreover, if settlement probabilities vary with flow characteristics, this can in turn influence foraging strategies that rely on fluid-mediated dispersal. Received: 9 January 1999 / Accepted: 8 June 1999     

Effects of temporal patterning of predation threat on movement of a stream fish: evaluating an intermediate threat hypothesis

The addition of nocturnal, Hoplias malabaricus, and diurnal, Crenicichla alta, predatory fishes downstream of barrier waterfalls increases predation threat for a killifish, Rivulus hartii, in Trinidadian streams. We hypothesized that the diel patterning of predation risk would affect prey movement rates, and tested this hypothesis by comparing movement in river sites/zones containing both the nocturnal and diurnal predator with movement in river sites/zones containing only the nocturnal taxon. We evaluated this prediction in the framework of an intermediate threat hypothesis (ITH) that holds that movement will be highest at some intermediate level of threat. We marked prey fish in study sites in two watersheds of a river, each with waterfalls that divided the river into three zones: a predator absent zone (P0), a zone with one nocturnal predator (P1), and a zone with one nocturnal and one diurnal predator (P2), and tested the ITH prediction that movement will be ordered as P0<P1>P2. The single predator promoted longitudinal movement by Rivulus (P0<P1), while zones with the two predators retarded movement for small Rivulus (P1>P2) as predicted by the ITH. However, movement by larger, less vulnerable Rivulus remained elevated (P1=P2 or P2>P1). A displacement experiment in each zone found that threat tended to reduce the probability of a displaced fish reaching home, but the two predator zones did not differ from one another in their effect on this probability. Hence, the prediction that predator activity over the full 24 h diel cycle would retard movement, P2<P1, was not supported with respect to homing. Because habitat and predator communities change predictably from headwater streams to larger rivers in many lotic ecosystems, we present a conceptual model for predicting fish movement behavior along this continuum. The model posits an important role for predation threat, and the size and spacing of refuge patches, suggesting that human alterations of these factors will affect the natural movement of fish in streams.     

Leech predation on juvenile freshwater snails: effects of size,species and substrate

Summary The leechGlossiphonia complanata does not appear to have substantial impact on snail populations, but this may be due to most studies focusing on adult snails rather than juvenile snails. In this study I investigated how predation rates ofG. complanata feeding on newly-hatched and juvenile snails was affected by snail species, snail size, snail density and substrate, in a laboratory experiment. Number of snails eaten increased with increasing density resulting in a type II functional response curve. Predation rates were higher when leeches were feeding onLymnaea emarginata than onPhysa gyrina, whereas there was no significant difference in predation rates when they were feeding onL. emarginata andHelisoma anceps. Sandy substrates and greater snail size resulted in decreased predation rates. Sand reduced movement speed ofG. complanata, which probably reduced encounter rates. Thus, there was a comparatively large effect of leech predation on newly-hatched snails, due to a high probability of encounter and high predation rates, but spatial and temporal refuges probably reduce the importance of leech predation as a structuring force in freshwater snail assemblages.     

Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and color

Predator-induced defenses are well studied in plants and invertebrate animals, but have only recently been recognized in vertebrates. Gray treefrog (Hylachrysoscelis) tadpoles reared with predatory dragonfly (Aeshnaumbrosa) larvae differ in shape and color from tadpoles reared in the absence of dragonflies. By exposing tadpoles to tail damage and the non-lethal presence of starved and fed dragonflies, we determined that these phenotypic differences are induced by non-contact cues present when dragonflies prey on Hyla. The induced changes in shape are in the direction that tends to increase swimming speed; thus, the induced morphology may help tadpoles evade predators. Altering morphology in response to predators is likely to influence interactions with other species in the community as well. Received: 17 April 1996 / Accepted: 18 September 1996     

Early male reproductive advantage,multiple paternity and sperm storage in an amphibian aggregate breeder

We tested whether the order in which males encounter females affects reproductive fitness in spotted salamanders (Ambystoma maculatum). Using mating chambers in the field, we allowed one male access to a female before a second male. We then used four microsatellite markers in paternity analyses of the resulting larvae. First males sired a significantly larger number of offspring than second males, suggesting that male reproductive success is greatly enhanced by early arrival at breeding ponds. Multiple paternity was common among clutches, and frequently larvae were assigned to unidentified males that had not been in the chambers. Sperm from these males had either been stored by females for a year or obtained more recently at other breeding sites.     

Density of an intraguild predator mediates feeding group size, intraguild egg predation, and intra- and interspecific competition

Intraguild predation (IGP) is common in most communities, but many aspects of density-dependent interactions of IG predators with IG prey are poorly resolved. Here, we examine how the density of an IG predator can affect feeding group size, IG egg predation, and the growth responses of IG prey. We used laboratory feeding trials and outdoor mesocosm experiments to study interactions between a social intraguild predator (larvae of the wood frog; Rana sylvatica) and its prey (spotted salamander; Ambystoma maculatum). Larvae of R. sylvatica could potentially affect A. maculatum by consuming shared larval food resources or by consuming eggs and hatchlings. However, successful egg predation requires group feeding by schooling tadpoles. We established from five to 1,190 hatchlings of R. sylvatica in mesocosms, then added either 20 A. maculatum hatchlings to study interspecific competition, or a single egg mass to examine IGP. Crowding strongly suppressed the growth of R. sylvatica, and IGP was restricted to the egg stage. In the larval competition experiment, growth of A. maculatum was inversely proportional to R. sylvatica density. In the predation experiment, embryonic mortality of A. maculatum was directly proportional to the initial density of R. sylvatica and the mean number of tadpoles foraging on egg masses. IGP on eggs reduced A. maculatum hatchling density, which accelerated larval growth. Surprisingly, the density of R. sylvatica had no overall effect on A. maculatum growth because release from intraspecific competition via egg predation was balanced by increased interspecific competition. Our results demonstrate that the density of a social IG predator can strongly influence the nature and intensity of interactions with a second guild member by simultaneously altering the intensity of IGP and intra- and interspecific competition.L . A. Burley and A. T. Moyer contributed equally to this work.     

Desiccation,predation, and mussel-barnacle interactions in the northern Gulf of California

Summary Field experiments were conducted in order to determine the potential for desiccation and predation to mediate the effect of mussels (Brachidontes semilaevis) on barnacles (Chthamalus anisopoma) in the highly seasonal northern Gulf of California. We did this by removing both mussels and a common mussel predator (Morula ferruginosa: Gastropoda) and by spraying selected sites with sea water during summertime spring low tides. We also determined the effect of crowding on resistance to desiccation in barnacles, and the effect of barnacles on colonization by mussels. The mussel-barnacle community was not affected by keeping experimental quadrats damp during daytime low tides throughout the summer. Exposure to summertime low tides, however, did affect the survivorship of isolated, but not crowded, barnacles; and barnacle clumps enhanced the recruitment of mussels. Hence crowding in barnacles had a positive effect on both barnacle survivorship and mussel recruitment. Morula had a negative effect on mussel density, and mussels had a negative effect on barnacle density. The effect of Morula on barnacle density was positive, presumably due to its selective removal of mussels. These results suggest an indirect mutualism between barnacles and the gastropod predator, because barnacles attract settlement or enhance the survival of mussels, and the predator reduces the competitive effect of mussels on barnacles.     

The impact of predation on the viburnum whitefly, (Aleurotrachelus jelinekii)

Summary In association with a detailed study of the population dynamics of the viburnum whitefly, Aleurotrachelus jelinekii, observations were made on the predators including spiders and five species of insect, notably the mirid Campyloneura virgula and the neuropteran Conwentzia psociformis. Although the species richness of the predator guild was positively correlated with prey population density, at the individual level there was little evidence over twelve years of a density dependent relationship. In these populations natural enemies do not seem to play an important role in the dynamics.     

Evidence for emergence of an amphibian iridoviral disease because of human-enhanced spread

Our understanding of origins and spread of emerging infectious diseases has increased dramatically because of recent applications of phylogenetic theory. Iridoviruses are emerging pathogens that cause global amphibian epizootics, including tiger salamander (Ambystoma tigrinum) die-offs throughout western North America. To explain phylogeographical relationships and potential causes for emergence of western North American salamander iridovirus strains, we sequenced major capsid protein and DNA methyltransferase genes, as well as two noncoding regions from 18 geographically widespread isolates. Phylogenetic analyses of sequence data from the capsid protein gene showed shallow genetic divergence (< 1%) among salamander iridovirus strains and monophyly relative to available fish, reptile, and other amphibian iridovirus strains from the genus Ranavirus, suggesting a single introduction and radiation. Analysis of capsid protein sequences also provided support for a closer relationship of tiger salamander virus strains to those isolated from sport fish (e.g. rainbow trout) than other amphibian isolates. Despite monophyly based on capsid protein sequences, there was low genetic divergence among all strains (< 1.1%) based on a supergene analysis of the capsid protein and the two noncoding regions. These analyses also showed polyphyly of strains from Arizona and Colorado, suggesting recent spread. Nested clade analyses indicated both range expansion and long-distance colonization in clades containing virus strains isolated from bait salamanders and the Indiana University axolotl (Ambystoma mexicanum) colony. Human enhancement of viral movement is a mechanism consistent with these results. These findings suggest North American salamander ranaviruses cause emerging disease, as evidenced by apparent recent spread over a broad geographical area.     

Use of plant resources by an omnivorous predator and the consequences for effective predation

Plant-provided food may enhance survival and establishment of omnivorous predators on target crops but on the other hand they may adversely affect predation rates and thus their potential for biological control of target pests. However, it is not known how predation is affected by plant food quality and prey density. The omnivorous predator Macrolophus pygmaeus is commonly used in augmentative releases in greenhouse crops. Experiments have shown its ability to utilize plant resources; eggplant and pepper plant leaves are the most and least suitable, respectively. In this study we searched the effects of floral resources (pollen or flower) of eggplant or pepper plant on the predation rate of M. pygmaeus. We used experiments in dishes (leaves) and cages (plants) under a range of densities of its prey, the aphid Myzus persicae. We did not find evidence that the consumption rates and the type of the functional responses of M. pygmaeus were affected by the plant leaf (eggplant vs pepper plant) or the increase in the spatial scale (leaf vs plant). However, the presence of pollen or a flower of eggplant and to a lesser extent of pepper plant reduced the plateau of the functional response to aphid density and increased the handling time per prey. The extent of prey feeding replacement by flower resources was dependent on the interaction between plant species and prey density. It seems that there is a constant rate of prey consumption replacement at intermediate and high prey densities on eggplant but only at intermediate prey densities on pepper plant. These results indicate the interactions between plant and prey resources in diets of omnivores and may be useful for its efficacy in pest control on eggplant and pepper plant.     

A continuous model of biomass size spectra governed by predation and the effects of fishing on them

A new time-dependent continuous model of biomass size spectra is developed. In this model, predation is the single process governing the energy flow in the ecosystem, as it causes both growth and mortality. The ratio of predator to prey is assumed to be distributed: predators may feed on a range of prey sizes. Under these assumptions, it is shown that linear size spectra are stationary solutions of the model. Exploited fish communities are simulated by adding fishing mortality to the model: it is found that realistic fishing should affect the curvature and stability of the size spectrum rather than its slope.     

Fungal infection alters the selection,dispersal and drift processes structuring the amphibian skin microbiome

Symbiotic microbial communities are important for host health, but the processes shaping these communities are poorly understood. Understanding how community assembly processes jointly affect microbial community composition is limited because inflexible community models rely on rejecting dispersal and drift before considering selection. We developed a flexible community assembly model based on neutral theory to ask: How do dispersal, drift and selection concurrently affect the microbiome across environmental gradients? We applied this approach to examine how a fungal pathogen affected the assembly processes structuring the amphibian skin microbiome. We found that the rejection of neutrality for the amphibian microbiome across a fungal gradient was not strictly due to selection processes, but was also a result of species‐specific changes in dispersal and drift. Our modelling framework brings the qualitative recognition that niche and neutral processes jointly structure microbiomes into quantitative focus, allowing for improved predictions of microbial community turnover across environmental gradients.     

Immunocytochemical localization and immunochemical characterization of an insulin-related peptide in the pancreas of the urodele amphibian,Ambystoma mexicanum

Summary The pancreas of the axolotl, Ambystoma mexicanum, was investigated by immunocytochemical methods for the presence of immunoreactivity to a number of antisera raised against mammalian insulins. All anti-insulin antisera tested revealed substantial amounts of reaction products confined solely to the aldehyde-fuchsinophilic B cells of the endocrine pancreas. The reactive cell population was detected by use of one polyclonal antiserum against bovine insulin and eight different monoclonal antibodies against insulins from various mammalian species. Six of these antibody clones have known specificity to sub-regions of the insulin molecule. Additionally, fractions of an ethanol-HCl extract of pancreatic tissue from Ambystoma was studied in both conventional dot-blot tests by means of the same panel of antibodies and a two-site sandwich time-resolved immunofluorometric assay for human insulin involving two of the monoclonal antibodies. These experiments support the immunocytochemical observations by demonstrating the existence of an insulin-related peptide with a great deal of structural resemblance to mammalian insulins and displaying antigenic determinants in common at least with the amino acid residues A_8–10 and B_26–30. In conclusion, we interpret the findings as indicating that the immunocytochemically revealed tissue bound antigen in the Ambystoma pancreatic B-cells may be a peptide related to human insulin.Supported in part by SNF grant 11-5082 (G.N.H.). The authors are indebted to Dr. P. Rosenkilde for the gift of the Ambystoma material     

Role of predation and parasitism in the extinction of the inoceramid bivalves: an evaluation

The inoceramid bivalves were dominant constituents of marine, epifaunal communities throughout the Late Mesozoic. They experienced a rapid decline in the Early Maastrichtian and virtually all taxa disappeared 1.5 Myr prior to the Cretaceous-Tertiary (K-T) boundary. The ultimate cause for their demise is still controversial. This study evaluates the role predation, parasitism and/or disease played in the evolution and extinction of Early Maastrichtian inoceramids from the Western Interior Seaway of North America (WIS). Escalation - the 'evolutionary arms race' between predators and prey - is said to be one of the most influential selective agents in evolution. Evidence of predation, parasitism, and disease in inoceramids is virtually undocumented prior to the Turonian. However, populations of inoceramids from the Late Cretaceous Pierre Shale show a marked increase in the number of individuals in which evidence for attempted predation and/or parasitism is preserved. The percentage of predation and/or parasitism steadily increases between the Baculites baculus and the B. grandis ammonite biozones (uppermost Campanian through Lower Maastrichtian) from 2.6% to values as high as 44.6%. The dramatic increase in shell deformities among inoceramids corresponds to a rapid radiation of shell-crushing brachyuran crabs and may be related to their activity. The introduction of new, efficient predators, such as brachyuran crabs, combined with parasitism and disease could have stressed inoceramid populations. Thus, they may have been more susceptible to environmental perturbations than under normal 'background' conditions. The disappearance of the inoceramids, at least from the WIS, may be one of the few cases where virtually an entire family lost the 'evolutionary arms race'.     

Multiple paternity in an aggregate breeding amphibian: the effect of reproductive skew on estimates of male reproductive success

Aggregate, or explosive, breeding is widespread among vertebrates and likely increases the probability of multiple paternity. We assessed paternity in seven field-collected clutches of the explosively breeding spotted salamander (Ambystoma maculatum) using 10 microsatellite loci to determine the frequency of multiple paternity and the number of males contributing to a female's clutch. Using the Minimum Method of allele counts, multiple paternity was evident in 70% of these egg masses. Simple allele counts underestimate the number of contributing males because this method cannot distinguish multiple fathers with common or similar alleles. Therefore, we used computer simulations to estimate from the offspring genotypes the most likely number of contributing fathers given the distributions of allele frequencies in this population. We determined that two to eight males may contribute to A. maculatum clutches; therefore, multiple paternity is a common strategy in this aggregate breeding species. In aggregate mating systems competition for mates can be intense, thus differential reproductive success (reproductive skew) among males contributing to a female's clutch could be a probable outcome. We use our data to evaluate the potential effect of reproductive skew on estimates of the number of contributing males. We simulated varying scenarios of differential male reproductive success, ranging from equal contribution to high reproductive skew among contributing sires in multiply sired clutches. Our data suggest that even intermediate levels of reproductive skew decrease confidence substantially in estimates of the number of contributing sires when parental genotypes are unknown.